Pucciniomycotina: Rust Fungi and Allies

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PucciniomycotinaRust Fungi and Allies

• General Mycology Pl P 421/521

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From Aime et al. 2006. Mycologia 98 896905.
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Taxa

• Pucciniomycetes
• Pucciniomycetesrust fungi
• Septobasidiales scale insect associates
• Platygloeales
• Helicobasidialesmonokaryon parasitic on rust
  fungi
• Microbotryomycetes anther smuts
• Other classes
• Atractiellomycetesgastroid, auricularioid
  species
• Cystobasidiomycetesyeast-like fungi, no
  basidiocarps
• Classiculomycetesaquatic fungi in freshwater
  habitats
• Mixiomycetesfern parasites
• Agaricostilbomycetesgastroid species, some
  yeast-like
• Cryptomycocolamycetesmycoparasite infecting
  ascomycete sclerotia

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From Aime et al. 2006. Mycologia 98 896905.
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Smut
Rust
Teliospore
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• 7000 species, 90 are rust fungi
• Most species are parasiticphytopathogens,
  mycoparasites, and entomopathogens
• Simple septa (monocot hosts) that lack caps, or
  poreless septa (dicot hosts)
• Phragmobasidia

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Pucciniomycetes Puccinales

• Rust fungi
• 7,000 species, 140-150 genera
• Most species are heterothallic
• Obligate biotrophs
• Intercellular hyphae with haustoria
• Most species form local infection
• Complex life cycles with up to five distinct
  spore types
• Many species require two unrelated hosts for
  completion of life cycle ( heteroecious)
• Some species complete life cycle on one host (
  autoecious)

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Spore states

• State 0 spermogonium bearing spermatia (n) and
  receptive hyphae (n)
• State I aecium bearing aeciospores (n n)
• State II uredinium bearing urediniospores (n
  n)
• State III telium bearing teliospores (n n ?
  2n)
• State IV basidium bearing basidiospores (n)

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Life cycles

• Macrocyclic
• All five spore states are present
• Demicyclic
• Uredinial state is absent ( spermatial state)
• Microcyclic
• Aecial and uredinial state is absent
  ( spermatial state)

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State 0 Spermagonium and spermatia (n)

• Result from infection by a haploid basidiospore
• Haploid state
• Small, pycnidial structures, often in clusters
• Develop in 4-6 days in herbaceous tissue, up to
  3-4 years in conifer wood
• 11 different types of spermagonia

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State 0 continued

• Receptive hyphae (flexuous hyphae) arise from
  upper walls and protrude through ostiole
• Spermatiasmall, one-celled, hyaline incapable
  of germination
• Spermatia in sweet, sticky exudate which attracts
  insects insects transmit spermatia
• Dikaryotization occurs when spermatium fuses with
  receptive hyphae nucleus moves down
  intercellular hyphae in host to aecial initials
• In species lacking spermagonium, dikaryotization
  through hyphal fusion

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Spermatia of Chysomyxa in sticky ooze. From
Common Tree Diseases of British Columbia, Pacific
Forestry Centre, B. C. http//www.pfc.forestry.ca/
diseases/CTD/Group/Rust/rust11_e.html
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State I Aecium and aeciospores (nn)

• Formed on same host as spermagonia
• Dikaryotization in aecial initials
• Aeciospores one-celled, usually verrucose, with
  germ-pores, and formed in chains, often with
  disjunctors usually pale orange in mass
• Chains of aeciospores usually surrounded by
  aecial peridium
• Aeciospores cannot infect same host on which they
  are produced in heteroecious rusts
• Infection by aeciospores results in uredinia (or
  telia in demicyclic rusts)

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SEM of aecia and aeciospores by Charles Mims
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Types of Aecia

• Caeoma
• Irregular outline due to lack of well-defined
  peridium
• Aecidium
• Cylindrical to cup-shaped with one-cell thick
  peridium
• Roestelia (in Gymnosporangium)
• Well-developed peridium, shreds longitudinally at
  maturity
• Peridermium (in Cronartium and Pucciniastrum)
• Flattened in one plane, resembling tongue or
  blister peridium several cells thick,
  fragmenting at maturity
• Uraecium
• Look like uredinia, but accupy position of aecia
  in life cycle aeciospores pedicillate, no
  peridium formed

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State IIUredinium and urediniospores (nn)

• Repeating state urediniospores able to re-infect
  host on which they are formed
• Formed on leaves, stems, fruit, fronds
  subepidermal becoming erumpent
• Urediniospores usually one-celled, echinulate,
  round to ovoid, with germ pores, formed on stalk
  (pedicillate)
• Sterile paraphyses in some taxa
• Germinate quickly, short-lived
• Amphispores thick-walled urediniospores
• Uredo form-genus if only uredinia are known

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Uredinial stage
SEM of uredinium and pedicillate urediniospore by
Charles Mims
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State IIITelium and teliospores (n n/2n)

• Teliospores form in uredinium (if present)
  usually not in woody tissue (except
  Gymnosporangium)
• Teliospores are site of karyogamy also referred
  to as probasidium
• Teliospores germinate by formation of basidium
  and basidiospores
• Teliospores have dormancy requirement in most
  species
• Teliospores provide basis for taxonomy

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State III continued

• Fourteen families recognized, primarily on basis
  of state III
• Melampsoraceae
• Teliospores united in subepidermal crusts or
  hornlike columns extending through host epidermis
• Pucciniaceae
• Teliospores pedicillate, formed on cushions or
  pulvinate masses that rupture host epidermis

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Telia and Teliospores
SEM by Charles Mims
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State IV Basidia and Basidiospores

• Diploid nucleus migrates into developing basidium
  ( metabasidium) and undergoes meiosis
• Septa formed in response to meiotic divisions (
  4-celled basidium)
• Each cell of basidium forms sterigmata
  basidiospores forcibly discharged
• Basidiospores germinate directly or indirectly
  germ tubes differentiate into appressoria when in
  contact with host cuticle

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Basidia and basidiospores
SEM by Charles Mims
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Melampsoraceae Pucciniastrum

• Telia consist of subepidermal crusts adhering
  laterally
• All species are heteroecious
• 0 and I on conifer needles
• II and III on Rosaceae and Ericaceae

Cummins and Hiratsuka. 1983. Illustrated Genera
of Rust Fungi.
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Pucciniastrum epilobi aecia on fir needles,
uredinia on fireweed leaf From Common Tree
Diseases of British Columbia. Pacific Forestry
Centre, B.C.
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Melampsoraceae Melampsora

• Telia subepidermal, laterally adhering
  teliospores one cell deep
• Heteroecious and autoecious species
• Heteroecious taxa
• 0 and I on conifer needles
• II and III on Populus and Salix

Cummins and Hiratsuka. 1983. Illustrated Genera
of Rust Fungi.
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Melampsoraceae Chrysomyxa

• Teliospores one-celled, catenate, germinating
  without dormancy
• Most species heteroecious
• 0 and I on Picea needles and cones
• III on Ericaceae or other dicots

Cummins and Hiratsuka. 1983. Illustrated Genera
of Rust Fungi.
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Chrysomyxa ledicola aecia on spruce needles.
From Common Tree Diseases of British Columbia.
Pacific Forestry Centre, B.C.
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Melampsoraceae Cronartium

• Telia subepidermal becoming erumpent as think
  columns of strongly adherent spores
• Teliospores one-celled, catenulate with pale
  walls, germinate without dormancy
• All species heteroecious
• 0 and I on cones stems
• II and III on various dicots
• Aecia of Peridermium type

Cummins and Hiratsuka. 1983. Illustrated Genera
of Rust Fungi.
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aeciospores
urediniospores
Cronartium ribicola aecia on white pine and
uredinia from Ribes. From Common Tree Diseases
of British Columbia. Pacific Forestry Centre,
B.C.
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Pucciniaceae Puccinia

• Teliospores two-celled, pedicillate, one germ
  pore per cell
• Infects most groups of vascular plants
• Heteroecious and autoecious species

Cummins and Hiratsuka. 1983. Illustrated Genera
of Rust Fungi.
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Puccinia asparagi telia and teliospores
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Pucciniaceae Uromyces

• Differs from Puccinia primarily in having
  one-celled teliospores
• Second largest genus, many species on legumes,
  also on members of composite, grass and lily
  families

Cummins and Hiratsuka. 1983. Illustrated Genera
of Rust Fungi.
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Pucciniaceae Hemileia

• 0 and I unknown
• III with distinctive urediniospores (humpbacked)
• One-celled teliospores, germinate without
  dormancy
• Most species are tropical
• H. vastatrix coffee rust

Cummins and Hiratsuka. 1983. Illustrated Genera
of Rust Fungi.
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Pucciniaceae Gymnosporangium

• Telia erumpent as cushions, crests or horns
  gelatinizing when wet mostly perennial on host,
  causing swellings
• Teliospores mostly two-celled, formed on
  gelatinizing pedicels, germinating without
  dormancy
• Aecia of Roestelia type
• Most species heteroecious, demicyclic
• 0 and I on dicots (esp. Rosaceae)
• III on conifers

Cummins and Hiratsuka. 1983. Illustrated Genera
of Rust Fungi.
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Cedar Apple Rust Aecia on Rosaceae, telial horns
on cedar
Photos by Al Black
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Gymnosporangium bethali teliospores, basidia and
basidiospores
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Pucciniaceae Phragmidium

• Teliospores usually phragmospores, formed on
  hygroscopic pedicels
• All species autoecious, most are macrocyclic
  occur on Rosaceae, mostly in Northern Hemisphere

Cummins and Hiratsuka. 1983. Illustrated Genera
of Rust Fungi.
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Phragmidium Telia and teliospores
Photos by Marco Hernandez-Bello
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Order Septobasidiales

• Obligately associated with scale insects (order
  Homoptera, superfamily Coccoidea)
• Predominately tropical and warm-temperate
• Dry, crustlike colony growing over insects forms
  thick-walled probasidium and septate metabasidium
• Basidiospores germinate on scale insects, form
  coiled haustoria inside insects
• Parasitized insects not killed, but prevented
  from reproducing
• Association is considered symbiotic
• Insects protected from parasitic wasps
• Fungus obtains nutrients from insect

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Septobasidium colony (Meredith Blackwell)
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Septobasidium illustrations from J. N. Couchs
The Genus Septobasidium
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Microbotryomycetes

• Now includes two orders of basidiomycetous yeasts
• Two families in Microbotryales formerly
  considered to be smut fungi

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Microbotryum

• Causes anther smut in Caryophyllaceae and other
  flowering plant families
• Induces anther formation in female flowers
• Characterized by violet-colored teliospores
• Insect transmitted
• Transversely septate basidium separates from
  teliospore

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Anther smut on Silene
Microbotryum illustrations from Kalman Vanky
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Jim Ginns Nightmare by Drew Parker